Flexor Burst Research Articles

Entrainment of the locomotor rhythm by group Ib afferents from ankle extensor muscles in spinal cats

1. Previous studies have concluded that the timing of the locomotor rhythm can be strongly influenced by input from group Ib afferents from leg extensor muscles (Duysens and Pearson 1980; Conway et al. 1987). The main objective of the present study was to obtain additional evidence for this conclusion by examining the characteristics of entrainment of the locomotor rhythm by rhythmic stimulation of group I afferents and by rhythmic force pulses in the ankle extensor muscles. 2. A reduced, non-immobilized preparation was developed in spinal cats that allowed isometric contractions of ankle extensor muscles to be elicited by ventral root stimulation during the expression of locomotor activity. The same preparation was used to examine the influence of electrically stimulating group I afferents from the ankle extensors and the effect of rhythmically stretching these muscles. The locomotor rhythm was initiated by sustained mechanical stimulation of the perineum following the administration of Clonidine and, in some preparations, Naloxone. 3. The timing of the onset of flexor burst activity was examined during entrainment with saw-tooth and ramp-and-hold stretches of the ankle extensor muscles. Flexor bursts were initiated about 200 ms following the release from the stretch, and this latency was independent of the entrainment frequency. 4. The locomotor rhythm was readily entrained by rhythmic contractions of the ankle extensor muscles produced by ventral root stimulation provided the magnitude of the contractions was greater than about 10N. Repetitive stimulation of group I muscle afferents from the ankle extensors also entrained the locomotor rhythm, with the timing of motor activity being similar to that during entrainment with rhythmic muscle contractions. Burst activity in the ipsilateral extensors was coincident with the stimulus trains in both cases. This similarity argues for entrainment being produced mainly by input from group Ib afferents. 5. The functional implication of the results of this and previous studies is that input from group Ib afferents during the stance phase of walking acts to inhibit generation of flexor burst activity and to promote extensor activity. The proposal that a decline in Ib activity near the end of the stance phase is involved in regulating the stance to swing transition is discussed.

Fictive motor patterns in chronic spinal cats

1. Fictive motor patterns were recorded in hind leg nerves of 10 adult chronic spinal cats (spinalized at T13). Four of these animals had been trained to step with their hind legs on a treadmill (late-spinal animals), whereas the remainder received no training and were examined a short time after spinalization (early-spinal animals). 2. A fictive pattern resembling the locomotor pattern for stepping was evoked in all animals in response to stimulation of the skin of the perineal region. (2-[2,6-Dichloroaniline]-2-imidazoline) hydrochloride (Clonidine) at doses ranging from 100 to 500 micrograms/kg iv facilitated the production of this pattern, particularly in early-spinal animals. 3. The fictive locomotor pattern in late-spinal animals was more complex than that occurring in early-spinal animals. In the latter the pattern consisted of an alternation of activity in flexor and extensor nerves, and changing leg position did not qualitatively alter the pattern, whereas in late-spinal animals the relative durations of the bursts in different flexors were usually not the same, and the pattern of flexor activity was dependent on leg position. 4. Moving the legs from extension to flexion progressively decreased the duration of flexor bursts, increased the cycle period, and decreased the ease with which the pattern could be evoked in both early- and late-spinal animals. 5. 1-beta-3,4-Dihydroxyphenylalanine (DOPA)/Isonocotinic acid 2-[(2-benzylcarbamoyl)ethyl]hydrazide (Nialamide) treatment following Clonidine in early-spinal animals increased the complexity of flexor burst activity. This, and other observations, indicates that DOPA and Clonidine do not have strictly identical actions on the locomotor pattern generator. 6. Stimulation of the paws in late-spinal animals produced two patterns of activity distinctly different from the locomotor pattern. of activity distinctly different from the locomotor pattern. One was a short sequence of high-frequency rhythmic activity (at approximately 8 c/s) in response to gently stimulating one paw with a water jet, and the other was a slow rhythm in flexor nerves in response to squeezing the paw. 7. The main conclusion of this investigation is that three distinctly different fictive motor patterns can be generated in chronic spinal cats depending on the method and site of stimulation. These patterns correspond to three different behaviors (locomotion, paw shake, and rhythmic leg flexion) that can be elicited in behaving chronic spinal cats in response to the same stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

Motor functions in rat hindlimb muscles following neonatal sciatic nerve crush

The sciatic nerve was crushed in the right hindlimb in newborn (3–8 h old) rats. Two to four months later, electromyographic activity was recorded from both the control and reinnervated ankle extensor muscles soleus or lateral gastrocnemius and from the ankle flexor muscle tibialis anterior. Tonic postural activity was present in the extensor muscles on both sides during quiet stance. The control flexor muscles were usually silent in this situation, but the reinnervated flexors exhibited abnormal sustained activity. During locomotion, the control extensors were activated during the stance phase and their mean burst made up 61.5% of the step cycle. The control tibialis anterior muscle fired only during the swing phase, with the burst lasting 18.1% of the step cycle. In the reinnervated extensor muscles, the mean burst duration was decreased (46% of the cycle) but the basic locomotor pattern was not impaired. The reinnervated tibialis muscle, however, was activated abnormally, with one appropriate flexor burst during the swing phase and an “extensor-like” burst during the stance phase of the step. Reflex responses to stretch were weak or absent on the operated side. Histological examination showed that the reinnervated soleus and tibialis muscles were almost devoid of muscle spindles. The motor unit mean firing rates in the reinnervated soleus (22 imp/s) and lateral gastrocnemius (45 imp/s) matched those of the control muscles (25 and 42 imp/s, respectively). In contrast to the phasic, high-frequency firing (52–80 imp/s) in the control tibialis, the reinnervated tibialis motor units fired at significantly lower rates (22–56 imp/s). Thus, neonatal sciatic nerve crush in rats markedly alters the activity pattern in fast flexors, such as the tibialis anterior, whereas the slow (soleus) and fast (lateral gastrocnemius) extensors are much less affected in this respect. The functional changes in the tibialis muscle may reflect increased motoneuron excitability, altered neuronal connectivity and/or lack of inhibition in the spinal cord, as a result of peripheral nerve lesion during a critical developmental period.

Locomotor activities in the decerebrate bird without phasic afferent input

We examined whether forelimb and hindlimb phasic afferent input is a prerequisite for the production of avian locomotor patterns. We eliminated phasic afferent feedback through paralysis of a decerebrate animal. The term “fictive” has been used to describe the neural activity associated with spontaneous or evoked motor output during neuromuscular paralysis. We observed that a paralysed decerebrate bird is capable of producing similar locomotor activity patterns as an unparalysed preparation, regardless of whether the “fictive” locomotion is generated spontaneously, or in response to focal electrical and/or neurochemical stimulation of discrete brainstem locomotor regions. Not all aspects of “fictive” locomotor patterns were identical to the locomotion elicited prior to paralysis. The stimulus current threshold necessary to evoke hindlimb locomotion increased from 69 ± 22 μ A (mean ± S.D.) prior to paralysis to 185 ± 87μ A for “fictive” stepping. For wing activity, the threshold increased from 84 ± 46 μ A during wing flapping to 228 ± 148μ A for “fictive” flight. In addition, the frequency of “fictive” efferent locomotor activity from the leg nerve (1.04 ± 0.44Hz) decreased relative to the frequency of leg activity prior to paralysis (1.55 ± 0.70Hz). Similarly, the frequency of wing activity decreased from 2.73 ± 0.73Hz before paralysis to 1.8 ± 0.69Hz after paralysis. Finally flexor burst duration remained constant during treadmill and “fictive” walking while the extensor burst duration was markedly increased during “fictive” walking. Thus, the relative contributions of leg flexor activity to the overall step cycle (burst proportion = burst duration/cycle duration) decreased during evoked “fictive” stepping, while the burst proportion of the leg extensor increased. Afferent feedback therefore appears to modulate leg extensor burst duration more than leg flexor duration. For the wings, the burst proportion of the major wing depressors remained constant before and after paralysis.

Activity of rubrospinal neurons during locomotion and scratching in the cat

It is now well established that locomotion and scratching in vertebrates can result from the activation of a spinal central generator. The possibility of control of these rhythmic motor activities by the red nucleus has been analyzed in the thalamic cat, in which efferent nerve discharges representing fictive locomotion or fictive scratching can still be recorded following paralysis by curarization. It was found that the discharge of lumbar-projecting rubrospinal neurons is modulated in relation to the intensity and frequency of the rhythmic efferent activity in the contralateral hindlimb. The average firing frequency was minimal at the transition between the extensor and flexor efferent bursts and increased progressively to reach a maximum in the second part of the flexor burst. Comparison of the rubrospinal activities during real and fictive rhythmic motor activities revealed only minor influences of phasic afferent inputs. Analysis of the relations between the rhythmic discharges found in rubrospinal neurons, cerebellar neurons (interpositus nucleus and paravermal Purkinje cells of the cerebellar anterior lobe) and neurons of an ascending pathway (ventral spinocerebellar tract) leads to the conclusion that the rubrospinal tract belongs to an internal loop between spinal and supraspinal centres. However, until now, the results do not allow the evaluation of its contribution to the motor performance, even in situations which, like those studied here, do not involve the complex motor control present in the intact cat.

Neuromuscular patterns of stereotypic hindlimb behaviors in the first two postnatal months. I. Stepping in normal kittens

Neuromuscular patterns associated with the development of hindlimb stepping behaviors were studied from birth to postnatal day 60 in normal kittens. Hindlimb muscles were chronically implanted with EMG electrodes at birth to characterize interlimb coordination and intralimb synergies during development of overground and treadmill stepping. Airstepping was also examined but seldom occurred after the second postnatal week. All kittens performed stepping under each condition, including weight-supported stepping, by postnatal day 3. The number of sequential steps on the treadmill and overground increased with age and cycle periods decreased. At onset, stepping behaviors were characterized by adult-like EMG patterns. Interlimb coordination was typified by alternating extensor bursts of similar duration. Extensors at the knee and ankle were coactive during the stance phase, and extensor burst durations were strongly correlated with the cycle periods over a wide range of stepping frequency. Ankle flexor and extensor muscles were reciprocally active during postural tremor, bouts of airstepping, and weight-supported steps on the treadmill and overground. The duration of the reciprocal flexor burst did not vary with cycle period or age. Observations of stepping behaviors and adult-like EMG patterns during initial postnatal development were contingent on optimal testing conditions. Taken together, the data suggest that pattern-generating circuits for regulating interlimb coordination and intralimb muscle synergies are potentially functional prior to the normal ontogenetic onset of locomotion. Perhaps the prolonged postnatal development of locomotion reflects the time required to establish adaptive mechanisms, such as postural control and agility, rather than spinal pattern-generating circuits for locomotion.

Proprioceptive input resets central locomotor rhythm in the spinal cat.

The reflex regulation of stepping is an important factor in adapting the step cycle to changes in the environment. The present experiments have examined the influence of muscle proprioceptors on centrally generated rhythmic locomotor activity in decerebrate unanesthetized cats with a spinal transection at Th12. Fictive locomotion, recorded as alternating activity in hindlimb flexor and extensor nerves, was induced by administration of nialamide (a monoamine oxidase inhibitor) and L-DOPA. Brief electrical stimulation of group I afferents from knee and ankle extensors were effective in resetting fictive locomotion in a coordinated fashion. An extensor group I volley delivered during a flexor burst would abruptly terminate the flexor activity and initiate an extensor burst. The same stimulus given during an extensor burst prolonged the extensor activity while delaying the appearance of the following flexor burst. Intracellular recordings from motoneurones revealed that these actions were mediated at premotoneuronal levels resulting from a distribution of inhibition to centres generating flexor bursts and excitation of centres generating extensor bursts. These results indicate that extensor group I afferents have access to central rhythm generators and suggest that this may be of importance in the reflex regulation of stepping. Experiments utilizing natural stimulation of muscle receptors demonstrate that the group I input to the rhythm generators arises mainly from Golgi tendon organ Ib afferents. Thus an increased load of limb extensors during the stance phase would enhance and prolong extensor activity while simultaneously delaying the transition to the swing phase of the step cycle.

Recovery and perturbation of paw-shake responses in spinal cats.

Paw-shake responses (PSRs) were evoked by wrapping masking tape around the hind-paw in nine cats spinalized at the T12 level either at 2 or 12 wk of age or as young adults (10-12 mo). Electromyographic responses of ankle extensors (LG and SOL) and one ankle flexor (TA) were recorded through the 6th mo after cord transection. Activity of the LG was used to determine the cycle characteristics. Cycle characteristics did not differ among cats spinalized at different ages. The average PSR, consisting of 11 cycles with a cycle time of 85 ms, was similar to the PSR of normal adult cats (16). Activity in the TA and LG muscles alternated with the onset of the flexor burst occurring at 52% of the extensor cycle. Burst durations averaged 39 and 57 ms for LG and TA muscles, respectively. Relatively normal PSRs were evoked within 48 h following cordotomy of the young-adult cats; differences being that the responses were elicited less frequently with fewer and slightly longer cycle times than normal. Within 2 wk following cord transection, PSR parameters returned to normal values. In the spinal cats, the SOL was active during PSR, showing either tonic low-level activity or discrete bursts that were coactive with the LG. In normal adult cats, the slow extensor (SOL) is usually inactive (16). In spinal cats, participation of the SOL may depend on a conversion of muscle units from slow to fast contracting (8, 13) or on the absence of inhibition of slow motor units from descending tracts (11). Both mechanisms are discussed.(ABSTRACT TRUNCATED AT 250 WORDS)

The effect of dorsal root transection on the efferent motor pattern in the cat's hindlimb during locomotion.

Mesencephalic cats can walk on a treadmill if the midbrain locomotor region is stimulated. The motor pattern of different hindlimb muscles is similar to that of th intact cat. The present experiments in the mesencephalic preparation test if the complex motor pattern in one hindlimb is causally dependent on the afferent signals arising in the same limb during walking. The electromyographical activity and the movement pattern during locomotion were compared before and after transecting all dorsal root fibres originating from one hindlimb. Flexor and extensor muscles at different joints may retain their general pattern after the dorsal root transection. This applies also to muscles such as the knee flexors, which have a short and early flexor burst and a second burst during the extension phase, and the short toe dorsiflexor , which has an early burst in the transition between flexor and extensor activity. After the dorsal root transection the pattern of activity may become more variable and it can even break down altogether. The present results demonstrate that the central nervous system devoid of phasic afferent inflow from one hindlimb can produce a complex motor output to this limb rather than a motor pattern degraded to a simple alternation between flexors and extensors.

Peripheral control of the cat's step cycle. II. Entrainment of the central pattern generators for locomotion by sinusoidal hip movements during "fictive locomotion.".

Acute low spinal and curarized cats injected with noradrenergic agonists i.v. can elicit an efferent burst pattern which can be recorded in muscle nerve filaments and can be referred to as "fictive locomotion". This study investigates the effect that feedback, arising from movements in the hip joint, can exert on the central network generating fictive locomotion. The central network is uncoupled from generating any active movements by curarization. The motor pattern could be entrained by applying sinusoidal hip movements, even when a very extensive denervation of the leg had been performed leaving only some of the muscles around the hip and the hip joint innervated. During flexion movements, efferents to different flexor muscles became active and during movements in the reverse direction (extension), efferents to extensors were active. With an increasing movement frequency the onsets of both flexor and extensor bursts were delayed in the movement cycle. The duration of the extensor bursts varied markedly with the movement cycle, whereas pure flexors changed less in burst duration. The frequency within which the efferent burst activity was entrained in a strict 1:1 relation to the movement varied between 5 to 70% above and below the resting burst period. In preparations with a narrow 1:1 range, a "relative coordination" was encountered outside this range. The flexor burst duration was in these cases dependent on where in the hip movement cycle the bursts appeared.

Peripheral control of the cat's step cycle. I. Phase dependent effects of ramp-movements of the hip during "fictive locomotion".

Acute spinal and curarized cats can generate "fictive locomotor activity" after an i.v. injection of Nialamid followed by 4-AP and L-DOPA. The efferent burst activity to flexors and extensors can be recorded in peripheral nerve filaments. Ramp-formed movements were applied in the hip at constant angular velocity in different phases of the spontaneous efferent burst activity. The cycle duration was markedly influenced. A flexion or an extension ramp applied in the early part of the "step-cycle" (during flexor activity) will prolong the cycle duration, but in the later part of the cycle instead a marked shortening effect will occur. The transition from a prolongation to a shortening is very steep for the extensive-ramps, with a subsequent gradual increase from a shortening to a lengthening of the cycle. This type of phase response curve expresses a potent peripheral modulatory effect on the central pattern generator. A ramp movement (flexion or extension) applied in the beginning of the flexor burst will reinforce the flexor activity. In the end of the flexor burst instead there is a directional sensitivity with positive feedback, resulting in an excitation of the flexor activity for flexion ramps, but a depression of the flexor activity for extension-ramps. Extension-ramps also show a position dependent effect which enhances the response in the flexors for more extended hip positions.

Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats

The role of proprioceptive input from the ankle extensor triceps surae in the control of walking was examined in premammillary cats walking on a treadmill. The left hindlimb was rigidly fixed in one position after denervating almost all the leg muscles except the ankle extensor (triceps surae) and ankle flexor (tibialis anterior). Rhythmic alternating contractions of the isolated ankle flexor and extensor occurred in the fixed hindleg during periods of walking in the other three intact limbs. These rhythmic contractions disappeared when the isolated triceps surae was stretched so as to increase the force of the active contractions to beyond 4 kg. With maintained stretch the periodic contractions in the ankle flexor and extensor returned only after the force in the stretched triceps surae gradually decreased and fell below approximately 4 kg. Isometric contractions of the triceps surae produced either by stimulation of ventral root S1 or by large amplitude vibrations also led to the sudden disappearance of ankle flexor bursts. Inhibition of the locomotory ryhthm could also be produced in all muscles of a single intact hindleg by clamping the ankle joint in a flexed position so as to stretch the ankle extensor. In all these cases, an increased rate of stepping of the contralateral hindleg was associated with the inhibition of the rhythmic locomotory activity. It is suggested that triceps surae proprioceptors signalling the presence of loading of the hindlimb extensor muscles inhibit the central generation of hindlimb flexion. During normal walking this mechanism could be of major importance during stance of prevent the initiation of the swing phase of a time when hindlimb extension is fully needed to support the weight of the animal. Thus a necessary, but not always sufficient, condition for the initiation of swing may be an unloading of leg extensor muscles.

Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats.

5. During the step cycle the peaks of both MG and SOL force profiles occur before the end of the yield (E2) phase, as both muscles undergo active lengthening. In contrast, peak MG and SOL forces during vertical jumping coincide with the end of active lengthening and the onset of ankle extensor shortening. 6. The results are consistent with the hypothesis that the inherent stiffness of active muscle during the step cycle is an important factor in the control of force output from hindlimb extensor muscles in locomotion. The division of labor between MG and SOL and the absolute force levels required from the MG during the full range of hindlimb movements in posture, locomotion, and jumping appear to be precisely matched to the very different characteristics of the motor-unit populations composing these synergistic muscles.

Reflex control of locomotion as revealed by stimulation of cutaneous afferents in spontaneously walking premammillary cats.

1. Stimulation of different hindlimb nerves in spontaneously walking premammillary cats was used in order to examine the effects of sensory input on the rhythmic motor output. 2. Stimulation of the tibial or sural nerve at low intensities caused the burst of activity in the triceps surae or semimembranosus to be prolonged if stimuli were given during the extension phase. When applied during the flexion phase, the same stimuli shortened the burst of activity in the pretibial flexors and induced an early onset of the extensor activity, except if stimuli were given at the very beginning of the flexion phase, when flexor burst prolongations or rebounds were observed instead. 3. These effects were related to activation of large cutaneous afferents in these nerves since the results could be duplicated by low-intensity stimulation of the tibial nerve at the ankle or by direct stimulation of the pad. 4. In contrast, activation of smaller afferents by high-intensity stimulation resulted prolongations of the flexor burst and/or shortenings of the extensor burst for stimuli applied before or during these bursts, respectively. 5. It was concluded that the large and small cutaneous afferents make, respectively, inhibitory and excitatory connections with the central structure involved in the generation of flexion during walking.

Motor Activity During Walking in the Cockroach Periplaneta Americana

ABSTRACT The patterns of electrical activity of selected muscles of the rear legs were studied during locomotion in unrestrained, freely moving cockroaches. During walking, muscle potentials in both extensor and flexor muscles were always grouped into bursts separated by periods of silence, with one burst occurring per step. During very slow walking, the occurrence of flexor and extensor bursts was synchronized with, respectively, the flexion and extension movements of the leg. At increasingly greater speeds of locomotion, the movements of the leg lagged increasingly behind the muscle activity, so that during very fast walking the extensor or flexor burst often began while the preceding leg movement was not quite half completed. ‘Slow’ extensor and’fast’ flexor bursts were studied in detail. The frequency of impulses within each extensor burst was usually steady, but sometimes declined in the middle or increased at the end of a burst. Frequency within’fast’ flexor bursts was often more varied, but there was no systematic change in frequency with any other parameter which was examined. For’slow’ extensor bursts, the duration of each burst, the number of impulses per burst and the mean interval between impulses in a burst each increased significantly as the duration of the associated step increased, i.e., there was a positive correlation between each pair of parameters. The rate at which the number of impulses per burst and mean interval per burst changed as a function of step duration was often significantly higher for steps shorter than about 300 msec than for longer ones. For’fast’ flexor bursts, the duration of each burst, the number of impulses per burst and the mean interval per burst were each extremely variable ; a weak correlation with step duration could only be demonstrated for the latter. However, both mean interval and the number of impulses per burst were positively correlated with the duration of the burst from which they were taken. The data qualitatively support current models of step generation in insects, but also suggest that a useful distinction could be made between very slow walking (below 3–4 steps per sec), termed ambling, and faster walking.